The geographical distribution of grey wolves (Canis lupus) in China: a systematic review

The grey wolf (Canis lupus) is one of the most widely distributed terrestrial mammals, and its distribution and ecology in Europe and North America are largely well described. However, the distribution of grey wolf in southern China is still highly controversial. Several well-known western literatures stated that there are no grey wolves in southern China, while the presence of grey wolf across China has been indicated in A Guide to the Mammals of China, published by Princeton University Press. It is essential to solve this discrepancy since dogs may have originated from grey wolfs in southern China. Therefore, we systematically investigated Chinese literatures about wild animal surveys and identified more than 100 articles and books that included information of the distribution of grey wolves in China. We also surveyed the collections of three Chinese natural museums and found 26 grey wolf skins specimens collected across China. Moreover, we investigated the fossil records of wolf in China and identified 25 archaeological sites with wolf remains including south China. In conclusion, with the comprehensive summary of Chinese literatures, museum specimens and fossil records, we demonstrate that grey wolves does distribute across all parts of the Chinese mainland, including the most southern parts of China.


INTRODUCTION
The grey wolf, Canis lupus, is one of the most widely distributed terrestrial mammals (Young & Goldman, 1944). Grey wolves live in a wide variety of habitats, including the dry Arabian desert, the xeric Mediterranean shrublands, the coniferous forests of Siberia, and the frozen tundra on Ellesmere island (Mech, 1981). Despite extirpation from many parts of their previous range over the last few hundred years, by persecution from humans and habitat fragmentation (Hunter & Barrett, 2011;Young & Goldman, 1944), wolves still retain most of their original distributions.
The distribution and ecology of grey wolves are largely well described in Europe and North America. However, in more peripheral and remote parts of their distributions, detailed information is often lacking. In the western literature, the wolf has generally been reported to be distributed throughout the northern hemisphere, from N15° latitude in North America and N12° latitude in India to beyond the Arctic Circle, but has been considered to be absent from Africa and the southern East Asia (Mech, 1981). However, recent articles reported that the Egyptian jackal (Canis aureus lupaster, Hemprich and Ehrenberg 1833) was not a subspecies of the golden jackal (Canis aureus, Linneaus 1758) and should be reclassified as the African wolf, Canis lupus lupaster (Gaubert et al., 2012;Koepfli et al., 2015;Rueness et al., 2001). 1 Similarly, the literature about wolves in China is limited outside China. This has led to misconceptions in the western literature about the distributions of wolves in China. Four studies, all conducted by western researchers, stated that wolf has never been presented in large parts of China (Callaway, 2013;Larson & Fuller, 2014;Nowak, 2003;Sokolov & Rossolimo, 1985 ).
However, as will be shown in this study the grey wolf has a historical and current range across nearly the entire country of China. There are more than 100 Chinese articles and books involving investigations of wolves in China since the 1950s (Table 1), showing the distributions in detail. Most of these articles are species investigations at a provincial or local level, however, there is no comprehensive description of the current distribution of wolves across China. Therefore, we here summarized the Chinese literature concerning past and present distributions of wolves in China, in order to synthesize data from this rich source of regional investigations into a comprehensive map of wolf distribution in China, and to make this significant information available to an international audience.  Shen et al., 2011-2001Sanjiang National Reserve Zhang et al., 2001-1999 Tangwanghe river forest distict He et al., 2003-1995Grand Khingan Zhang et al., 1998a-1989-1995Northern Grand Khingan Li et al., 1996, 1987-1990, 1992 Xingkai Lake Nature Reserve Li et al., 1993Li et al., 1971Li et al., -1980Li et al., , 1981Li et al., -1990 Heilongjiang province Zhang et al., 1998b N/A Heilongjiang province Zhang & Yu, 2005 N/A Western Helongjiang province Gao et al., 1999Jilin 1992Yanbian Qiu et al., 19951992Hunjiang Li et al., 1994Liaoning 1999Nuluerhusan National Reserve Zhou et al., 2007Benxi Zhao et al., 2004a 37 counties in Liaoning province Zhao et al., 2004b-1999 Xinjiang 1994Kanas National Nature Reserve Abdukadi et al., 19991987Wuqia, Taxkorgan, Yecheng, Qiemo, Yutian Feng, 19901965, 1980, 1983, 1985 Zhungeer & Altai Zhang & Hu, 19881979 Xinjiang Gao, 1997bGao, 1958Gao, -1961 Desert plains area in Xinjiang Zhang, 1963 Li et al., 2007Shandong 1984-1987 Jiaodong peninsula Sun, 19881982-1986Qingzhou Cong, 19881961-1966, 1973 Jiaodong and Luzhongnan area Lu, 1984 N/A Laoshan Tian et al., 2000Anhui 1959-1964 Anhui province Wang et al., 1966 N/A Anhui province Wu et al., 2002 N/A Huangshan Xu, 1997 Jiangsu N/A Jiangsu province  Zhejiang

LITERATURE SUMMARIZATION
It is controversial to describe the distribution of grey wolves in western literatures. Two articles reported that wolves were previously present all across China, but is now extinct from southern China (Ginsberg & Macdonald, 1990;Lau et al., 2010). In four well-known studies, researchers claimed that wolves have never existed in sourthern China (Callaway, 2013;Larson & Fuller, 2014;Nowak, 2003;Sokolov & Rossolimo, 1985), suggesting that sourthern China cannot be the harbor of dog domication. Thus, southern China is usually treated outside the range of wolf distribution (IUCN; EOL). However, in 2008, Smith and his colleagues described the distribution of wolf in China, indicating that grey wolves were present all across the mainland of China (Smith & Xie, 2008 Fujian province, in Longzhou, Ningming, and Shangsi of Guangxi, in Guangdong province, in Guizhou province, in Lushui and Chengkou of Yunnan, in Yumen, Zhangye, and Linxia of Gansu, in Menyuan, Qilian, Alaer, Golmud, and Delingha of Qinghai, in Pali, Nylamu, Tingri, Shigatse, and Naqu of Tibet, and in Shiqu, Ruoergai, Songpan, Leibo, Ebian, Kangding, Wanxian, Yibin, and Mianyang of Sichuan" (Gao & Wang, 1987).

WOLF SKINS IN ZOOLOGICAL MUSEUMS
In addition to the literature investigation, we made a survey of wolf skins in the archives of the National Zoological Museum of China, Kunming Natural History Museum of Zoology, and Shaanxi Institute of Zoology, and (Table 2, Figure 2, Figure 3).
We found 26 wolf skins sampled from 13 provinces across China, e.g., two specimens sampled from two southern Chinese provinces (Zhejiang and Fujian) in 1974, and one from southern Yunnan in 1985.

WOLF FOSSIL RECORD
We investigated the literature about archaeological research in China, to identify information about wolf fossils in archaeological sites. We extracted information about the fossil record of the grey wolf in China from three Chinese books (Lv, 2004;Yuan, 2015;Zhang et al., 2003). These books reported 25 archaeological sites in 14 provinces across China with wolf fossils records (Table 3), including the 12 000 years old remains from the South Chinese province Jiangxi.

DISCUSSION
In this study, we showed that contrary to what is reported in many references in the western literature, the grey wolf actually is present across virtually all parts of the mainland China. This correction is important in studies of wolf ecology and conservation. It gives a correct picture of the worldwide Figure 2 Source and geographical origin of museum wolf skin specimens distributions of wolves, by filling in a large blank region on the map. It is also important in studies of the history of domestic dogs, since dogs probably trace a large proportion of their genetic ancestry to wolves from the southern parts of East Asia (Wang et al., 2016). The wolf has endured massive decline in population size and geographic range around the world during the previous two centuries, because of human influence including habitat loss, persecution, hunting (for obtaining, e.g., trophies, furs and material for traditional medicine), and depletion of prey (Beschta & Ripple, 2010;Callan et al., 2013;Levi & Wilmers, 2012;Ripple et al., 2014). Also in China, the distribution areas of wolves have severely decreased due to human mediated habitat loss and hunting (Gao, 1997a(Gao, , 2006Zhang, 1999). Official investigations from the middle of the 20th century reported that wolves were distributed in every province of China except some islands, but gave no exact numbers. Today, large populations remain only in the northwestern and northeastern parts of the country, Inner Mongolia and Tibet, but even in these regions, the numbers are relatively small, e.g., only 2 000 wolves in Inner Mongolia were reported in the 1990s (Gao, 1997a). We have here shown that wolves still seem to be present across all parts of the Chinese mainland, including the most southern provinces. Thus, even though habitat loss has been severe in urban and agricultural regions, wolves seem to have persisted in intervening regions.
The data about wolf distributions that we here present were investigations on either provincial or local level, whereas, a comprehensive ecological survey of the wolves in China. It is therefore not clear how the wolf populations in the different parts of China are interrelated. For example, it is not clear whether wolves recorded in the southern provinces represent permanent populations, or a steady stream of individuals migrating from the northern provinces. However, it is notable  Table 2), Jiangxi Province (middle, ID 23 in Table 2) and Shaanxi Province (right, ID 24 in Table 2).  Guangdong and Guangzhou in 2000. These findings indicate a consistent presence of permanent populations across southern China. Moreover, to obtain a comprehensive picture of the status of the wolves in China, it is necessary to carry out both ecological and genetic studies, e.g., in concerning the genetic relationships either among the wolf populations across China and between these and worldwide wolf populations. This study points out misconceptions in the western literature about the distributions of wolves in China. The origin of this problem is not clear, but it can be traced back as far as an article in 1985 from which the factoid has, stepwise, been passed on to other articles (Sokolov & Rossolimo, 1985). It is probably because of the linguistic barrier to the Chinese literature that this error has previously not been pointed out. This case can be explained by inefficient research in peripheral parts of the species distribution, in countries with limited resources. Our study raises the question whether this kind of misconceptions also exist in other species than just the grey wolf.

CONCLUSIONS
With a comprehensive summary of Chinese literature, specimens and fossil records, we showed that wolves are present across all parts of the Chinese mainland, including the southern parts. Hereby we corrected an error in western literature, in which most sources stated that wolves were not present in the southern China, and some even claimed that wolves have never been presented there, even in ancient times. There is no comprehensive description of the current distributions of wolves across China, and therefore this study serves both to give an updated description of wolf distributions in China, and to make this significant information available to an international audience.